Pesq. Vet. Bras.

35(1):89-94, janeiro 2015

DOI: 10.1590/S0100-736X2015000100017

Characterization of the estrous cycle in Galea spixii

(Wagler, 1831)1
Amilton C. Santos2, Diego C. Viana2, Bruno M. Bertassoli3, Gleidson B. Oliveira4,
Daniela M. Oliveira2, Ferdinando V.F. Bezerra4, Moacir F. Oliveira4
and Antônio C. Assis-Neto2*

ABSTRACT.- Santos A.C., Viana D.C., Bertassoli B.M., Oliveira G.B., Oliveira D.M., Bezerra
F.V.F., Oliveira M.F. & Assis-Neto A.C. 2015. Characterization of the estrous cycle in Galea
spixii (Wagler, 1831). Pesquisa Veterinária Brasileira 35(1):89-94. Setor de Anatomia dos
Animais Domésticos e Silvestres, Faculdade de Medicina Veterinária e Zootecnia, Univer-
sidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, SP 05508-030,
Brazil. E-mail: antonioassis@usp.br
The Galea spixii inhabits semiarid vegetation of Caatinga in the Brazilian Northeast. They
are bred in captivity for the development of researches on the biology of reproduction. The-
refore, the aim of this study is characterize the estrous cycle of G. spixii, in order to provide
information to a better knowledge of captive breeding of the species. The estrous cycle was
monitored by vaginal exfoliative cytology in 12 adult females. After the detection of two
complete cycles in each animal, the same were euthanized. Then, histological study of the
vaginal epithelium, with three females in each phase of the estrous cycle was performed;
five were paired with males for performing the control group for estrous cycle phases, and
three other were used to monitor the formation and rupture of vaginal closure membrane.
By vaginal exfoliative cytology, predominance of superficial cells in estrus, large intermedia-
te cells in proestrus, intermediate and parabasal cells, with neutrophils, in diestrus and me-
testrus respectively was found. Estrus was detected by the presence of spermatozoa in the
control group. By histology, greater proliferation of the vaginal epithelium in proestrus was
observed. We conclude that the estrous cycle of G. spixii lasts 15.8 ± 1.4 days and that the va-
ginal closure membrane develops until complete occlusion of the vaginal ostium, breaking
after few days. Future studies may reveal the importance of this fact for the reproductive
success of this animal.
INDEX TERMS: Galea spixii, cavies, female, preservation, reproduction, rodents.

RESUMO.- [Caracterização do ciclo estral de Galea spixii gia da reprodução. Sendo assim, o objetivo deste trabalho
(Wagler, 1831).] Os Galea spixii habitam a vegetação semiá- foi caracterizar o ciclo estral de G. spixii para obtenção de in-
rida da Caatinga, no Nordeste brasileiro. Eles são criados em formações que melhorem o conhecimento do manejo repro-
cativeiro para realização de pesquisas relacionadas a biolo- dutivo da espécie em cativeiro. O ciclo estral foi monitorado
por citologia esfoliativa vaginal em doze fêmeas adultas.
1
Received on April 1, 2014. Após a detecção de dois ciclos completos em cada animal, os
Accepted for publication on December 21, 2014. mesmos foram eutanasiados. Em seguida foi realizado estu-
2
Faculdade de Medicina Veterinária e Zootecnia, Universidade de São do histológico do epitélio vaginal com três fêmeas em cada
Paulo (USP), Av. Prof. Dr. Orlando Marques de Paiva 87, Cidade Univer- fase do ciclo estral; cinco foram pareadas com machos para
sitária, São Paulo, SP 05508-270, Brazil. E-mails: amiltonsantoss@bol.
com.br, diegoviana@usp.br, oliveiradm@usp.br; *Corresponding author: realização do grupo controle e outras três fêmeas foram uti-
antonioassis@usp.br lizadas para monitorar a formação e ruptura da membrana
3
Universidade Federal de Minas Gerais (UFMG), Av. Presidente Antônio de oclusão vaginal. Através de citologia esfoliativa vaginal,
Carlos 6627, Belo Horizonte, MG 31270-901, Brasil. E-mail: brunobertassoli@ constatou-se predomínio de células superficiais em estro,
gmail.com
4
Universidade Federal Rural do Semi-árido, BR-110 Km 47, Mossoró, RN
células intermediárias grandes em proestro, células inter-
59625-900, Brazil. E-mails: gleidson_benevides@hotmail.com, moacir@ mediárias pequenas e células parabasais com presença de
ufersa.edu.br neutrófilos em diestro e metaestro, respectivamente. O es-

89
90 Amilton C. Santos et al.

tro foi detectado pela presença de espermatozoides no gru- 2028236/2008) and Bioethics Committee of the School of Veteri-
po controle. Através de histologia, observou-se uma maior nary Medicine and Animal Science of the University of São Paulo,
proliferação no epitélio vaginal no proestro. Concluiu-se Brazil (protocol 2400/2011).
que o ciclo estral de G. spixii dura em média 15.8 ± 1.4 dias e Detection of estrous cycle phases by vaginal cytology.
Twelve adults, non-pregnant females in three separate boxes,
a membrana de oclusão vaginal se desenvolve até completa
each of which contained four properly identified females were
oclusão do óstio vaginal externo, rompendo-se em poucos used. During the experiment the females were fed with fruits,
dias. Futuros estudos podem revelar a importância deste úl- grasses, corn, rabbit feed and water.
timo fato para o sucesso reprodutivo deste animal. In another box, five females were paired with adult males for
TERMOS DE INDEXAÇÃO: Galea spixii, fêmeas, preás, preservação, comparison of cell types along the estrous cycle, especially in the
reprodução, roedores. estrous phase, with possible detection of spermatozoa in vaginal
exfoliative cytology.
INTRODUCTION The vaginal exfoliative cytology was performed daily by the
same collector. The collection of vaginal smears was performed
The Spix’ yellow-toothed cavies (Galea spixii) are rodents using swabs of sterile cotton and subsequent deposit of biological
that belong to the Caviinae subfamily and Caviidae family. material in histological slides, which were stained with fast Pa-
They live in semiarid vegetation of Caatinga at Brazilian noptic, according to the manufacturer (Laborclin®, Vargem Gran-
Northeast (Oliveira et al. 2008), where they are constantly de/Pinhais, PR, Brazil). The females were independently monito-
used as alternative source of protein for inhabitants of this red and there was no synchronization.
region (Santos et al. 2014a). Subsequently, the samples were analyzed and photo docu-
In Brazil, they are bred in captivity for conservation of the mented by light microscopy. Different cell types: superficial cells;
species, which is found as vulnerable in the “red list of threate- large and small intermediate cells; parabasal cells and neutro-
phils were identified (Stockard & Papanicolaou 1917, Selle 1922,
ned species” (IUCN 2014). Moreover, they are used for develo-
Lilley et al. 1997, Touma et al. 2001, Allison et al. 2008).
pment of a new experimental model for research about repro- For a better monitoring of the estrous cycle phases, cells were
ductive biology (Rodrigues et al. 2013, Santos et al. 2014b). counted in each sample of vaginal exfoliative cytology into fields
Researches related with reproductive biology have sho- containing from 0 to 100 cells in the cytological slides (Guimarães
wn that G. spixii has continuous poliestral cycle, developing et al. 1997). During the counting, cell types were grouped accor-
a type of inverted choriovitellinic placenta during pregnancy ding to the criteria of morphology of each cell as above described.
(Oliveira et al. 2008, 2012); gestation period lasts about 48 After counting of two complete estrous cycles, average of the
days (Oliveira et al. 2008); the onset of puberty in males oc- estrous cycle length of each female; of the females that showed es-
curs after 45th postnatal day (Santos et al. 2012); and females trous cycle of the same duration; and, finally, the average of all fema-
have masculinized external genitalia (Santos et al. 2014b). les were established. Statistical analysis was applied to the Student-
It is known that the majority of female rodents can -t test for paired and unpaired values, with p < 0.05 of significance.
Day 1 was established by absence of neutrophils and predo-
breed throughout the year and the reproductive cycle is
minance of superficial cells (Allison et al., 2008); and by observa-
systematically repeated, alternating periods of sexual acti- tion of copulation in the control group.
vity and preparation of the reproductive tract for possible Monitoring of the development and rupture of the vagi-
pregnancy (Selle 1922, Lilley et al. 1997, Touma et al. 2001, nal closure membrane. In this phase of the experiment, another
Mahoney et al. 2011). In this sense, tools to detect features box containing three females, isolated from males were used. We
related to receptivity of the female for copulation in order started the analysis after observation of rupture of vaginal closu-
to assist captive breeding of threatened species is very im- re membrane. Development of vaginal closure membrane in all
portant (Binelli et al. 2014). females was monitored until complete occlusion of the external
Regarding Caviidae as Cavia porcellus (Stockard & Papa- vaginal ostium, ending at the moment of rupture. In this group,
nicolaou 1917; Kelly & Papanicolaou 1927), C. aperea and vaginal cytology was not used to avoid mechanical rupture of the
vaginal closure membrane. Photo documentation was performed
G. musteloides (Touma et al. 2001), the authors report that
by camera Olympus SP 810UZ 14 mp.
females show development of a vaginal closure membrane Histological analysis of the vaginal epithelium during the
during the estrous cycle. This fact may be related to intras- estrous cycle phases. After analysis of the estrous cycle by vagi-
pecific sexual selection and formation of various mating nal cytology, the 12 females separated from males were anesthe-
systems among Caviidae (Adrian & Sachser 2011). tized with xylazine (4mg/kg/IM) and ketamine (60mg/kg/IM),
Due to the lack of studies on the reproductive cycle of and then euthanized with sodium thiopental (2.5% 60mg/kg) by
G. spixii females, characterize the estrous cycle by vaginal intracardiac cannulation. Three females were in estrus; three in
exfoliative cytology and corresponding vaginal epithelium proestrus; three in diestrus; and three in metestrus.
variations and check the presence of vaginal closure mem- Vaginal tissue samples from all females were fixed in 10% for-
brane, providing more data for captive breeding of this spe- malin solution, processed for light microscopy and stained with
H/E (hematoxylin/eosin). Microscopic photodocumentation was
cies were the aim of this study.
performed using BX61VS Olympus photomicroscope.

MATERIALS AND METHODS

RESULTS
Animals. Twenty adults, non-pregnant, primiparous females
and two adult males, prevenient of the Center for Wild Animals Detection of the phases of the estrous cycle by vaginal
Multiplication of Federal Rural University of the Semi-Arid, Mos- exfoliative cytology
soró, RN, Brazil were used. This research was approved by Brazi- The cell types found by vaginal exfoliative cytology
lian Institute of Environment and Renewable Resources (IBAMA, were: (1) parabasal cells, which were small and round,

Pesq. Vet. Bras. 35(1):89-94, janeiro 2015

 Characterization of the estrous cycle in Galea spixii (Wagler, 1831) 91

with a central nucleus occupying an area greater than the copulation, females followed pregnancy. The vaginal exfo-
cytoplasm; (2) small intermediate cells, which were ovoid, liative cytology in this group showed that, in estrus phase,
with a central nucleus smaller than the cytoplasm; (3) enucleated superficial cells and superficial cell with pic-
large intermediate cells, which were polygonal cells, with notic nuclei were predominant, and neutrophils were not
a nucleus smaller than the cytoplasm, when compared to found. Prior estrus, we observed predominance of large
small intermediate cell; and (4) superficial cells with three intermediate cells, which gradually were replaced by su-
different morphologies: nucleated, enucleated, and with perficial cells (Fig.1).
picnotic nucleus (Fig.1). In addition, polymorphonuclear
neutrophils were also found.

Fig.1. Cell types by vaginal exfoliative cytology in Galea spixii. (A)

Superficial nucleated cells (arrows), proestrus; (B) enuclea-
ted superficial cell (arrow), estrus; (C) superficial cells with
picnotic nuclei (arrow) and spermatozoa (arrowhead), estrus;
(D) parabasal cell (arrow) and neutrophils (arrowhead), me-
testrus; (E) large intermediate cells (filled arrow), small in-
termediate cells (white arrowhead), parabasal cells (empty
arrow), and neutrophils (black arrowhead), diestrus. Bars =
100µm.

We observed that the amount of these different cell

types varied in each phase of the estrous cycle. During es-
trus, there was a predominance of superficial cells, which
went from nucleated to enucleated. In metestrus, there
was predominance of parabasal cells with presence of lar-
ge numbers of neutrophils. Superficial and intermediate
cells were also present in this phase. In diestrus there was
predominance of small and large intermediate cells, with
presence of neutrophils and parabasal cells. In proestrus,
there was predominance of large intermediate cells and su-
perficial cells, with little or no presence of neutrophils. We
found six different estrous cycle lengths (Fig.1 and 2). Fig.2. (A) Percentage of parabasal cells, (B) small intermediate
In the control group, the cell types were the same as cells (C) large intermediate cells, and (D) superficial cells by
those found in the experimental group, but the duration of vaginal exfoliative cytology, reflecting different estrous cycle
the estrous cycle could not be found, because of the copula, durations in Galea spixii. Day 1 includes the onset of estrus,
which interrupted the experiment. Copulation was confir- while days 14, 15, 16, 17, 18 and 19 indicate the last day of
med by presence of spermatozoa in vaginal smears. After proestrus.

Pesq. Vet. Bras. 35(1):89-94, janeiro 2015

92 Amilton C. Santos et al.

Fig.3. Modifications in vulva and clitoris of Galea spixii. (A) Vulva (black arrow) with broken vaginal closure membrane (arrow) and
clitoris (empty arrow); (B) vulva (black arrow) with partially developed vaginal closure membrane (arrow) and clitoris (empty
arrow); (C) vulva (black arrow) with fully developed vaginal closure membrane (arrow) and clitoris (empty arrow). Bars = 1cm.

epithelium underwent proliferation, cornification and cell

desquamation along the estrous cycle. In estrus phase, va-
ginal epithelium contained one or a few layer of cornified
superficial cells. After the estrus phase (metestrus), the
epithelium lost the superficial cells. Then, the epithelium
presented one or a few parabasal layers. In diestrus, the
epithelium initiated the cell proliferation, consisting on
evident stratified epithelium. In proestrus, epithelium un-
derwent massive proliferation. Then, the outer cells began
the cornification process, with the approximation of next
estrus (Fig. 4).

Estrous cycle length by vaginal exfoliative cytology

We found females with estrous cycle ranging between
14 and 18 days with a mean of 15.6 ± 1.3 days in the first
estrous cycle. In the second estrous cycle, we found females
with cycles ranging between 14 and 19 days, with mean of
Fig.4. Vaginal epithelium of Galea spixii. (A) Stratified epithelium 16.1 ± 1.5 days. The average of two complete cycles was
in diestrus (arrow); (B) stratified epithelium with cornifica- 15.8 ± 1.4 days. The Student-t test for paired samples sho-
tion in proestrus (arrow); (C) superficial epithelial cells (cor- wed no difference between cycles (p<0.05).
nified) in estrus (arrow); (D) epithelium with less stratified
epithelium in early metaestrus (arrow). HE, Bars = 200μm. DISCUSSION
Development and rupture of the vaginal closure mem- Understanding the reproductive behavior of animals can
brane contribute to the development of techniques and tools for
The development of vaginal closure membrane was the biotechnology of reproduction, including artificial inse-
observed in those three females separated from males. In mination, in vitro fertilization, embryo transfer and cryo-
these females, the membrane developed gradually, blocking preservation in several species bred in captivity, in order to
the external vaginal ostium, and then, naturally, this mem- ensure better reproductive performance and preservation
brane ruptured within a few days. During a first moment, of genetic variability (Domingues & Caldas-Bussiere 2007,
vaginal closure was broken. In few days, this membrane be- Guimarães et al. 2011, Binelli et al. 2014).
gins to grow and occlude the external vaginal ostium. Then, Thus, in the present study, we found satisfactory results
this membrane completely occludes the external vaginal os- for detection of estrous cycles by vaginal exfoliative cytolo-
tium, giving an aspect of absent external vaginal ostium dur- gy, and there was no statistical difference (p<0.05) betwe-
ing this period. Then in few days, vaginal closure membrane en the duration of the first and second estrous cycles. In
breaks again. These events occurred cyclically (Fig. 3). addition, histological tests confirmed the results found in
vaginal exfoliative cytology. The histological analysis sho-
Histological analysis of the vaginal epithelium through- wed cell proliferation and cornification more pronounced
out the estrous cycle in proestrus and estrus, as found in Cavia porcellus (Sto-
By histological studies, data performed by vaginal exfo- ckard & Papanicolaou 1917) and Lagostomus maximus
liative cytology were confirmed. We found that the vaginal (Weir 1971). In this sense Deanesly (1966) showed that

Pesq. Vet. Bras. 35(1):89-94, janeiro 2015

 Characterization of the estrous cycle in Galea spixii (Wagler, 1831) 93

estradiol and sometimes small amount of androstenedio- Table 1. Estrous cycle duration in different rodent species
ne combined with estradiol stimulated cell proliferation. In Species Author Duration
other hand, progesterone combined with estradiol showed (days)
negative results for epithelial proliferation in vagina of Ca- Caviinae Galea spixii Current research 15.8±1.4
via porcellus. subfamily Cavia porcellus (Stockard & 15-17
In G. spixii, the predominant cell types in the different Papanicolaou 1917)
phases of the estrous cycle were easier to detect during the Cavia aperea (Touma et al. 2001) 15
proestrus and estrus by vaginal exfoliative cytology, similar Microcavia australis (Adrian & Sachner 2011) 15
Others, Dasyprocta (Guimarães et al. 2011) 25-40
to that found in other rodents such as Cavia porcellus (Sel-
family and prymnolopha
le 1922, Lilley et al. 1997) Dasyprocta prymnolopha (Gui- subfamily Dasyprocta (Guimarães et al. 1997) 19-40
marães et al. 1997), Agouti paca (Guimarães et al. 2008) of rodents prymnolopha
and Myocastor coypus (Felipe et al. 2001). Our results also Agouti paca (Guimarães et al. 2008) 24-42
agree with those described in domestic mammals (Allison Octodon degus (Mahoney et al. 2011) 17-22
Myocastor coypus (Felipe et al. 2001) 20-60
et al. 2008). Lilley et al. (1997) showed positive correlation Thryonomys (Addo et al. 2007) 27.8 ± 22.1
between vaginal impedance measurements and vaginal swinderianus
exfoliative cytology used for monitoring of estrous cycle in Rattus norvegicus (Marcondes et al. 2002) 4-5
Cavia porcellus. Mus musculus (Mendonça et al. 2007) 4
We believe that the satisfactory detection of estrous
cycle phases was possible due to the fact of G. spixii presents Females of G. spixii have short and regular estrous cycle
continuous poliestral cycle (Oliveira et al. 2008) similar with duration close to that found in other rodents belon-
that found in other rodents, as Myocastor coypus (Felipe et ging to the Caviinae subfamily, as Microcavia australis
al. 2001), Dasyprocta prymnolopha (Guimarães et al. 2011), (Adrian & Sachser 2011), Cavia aperea (Touma et al. 2001)
Agouti paca (Guimarães et al. 2008), Paca cuniculus (Reis and Cavia porcellus (Selle 1922, Lilley et al. 1997). To sim-
et al. 2011) and Rattus norvegicus (Marcondes et al. 2002). plify comparison, in Table 1 we highlighted the duration of
Galea spixii showed formation of the vaginal closure the estrous cycle in different rodents.
membrane, which can also be found in other rodents, as The continuous poliestral cycle and short gestational
Thryonomys swinderianus (Addo et al. 2007), Lagostomus period (Oliveira et al. 2008), associated with short estrous
maximus (Weir 1971), Galea musteloides and Cavia aperea cycles found in G. spixii females in this present study may
(Touma et al. 2001), Octodon degus (Mahoney et al. 2011), be related to the reproductive success of this species (Pur-
Cavia porcellus (Selle 1922, Lilley et al. 1997) and Rattus ves et al. 2005) as found in others rodents which belong to
norvegicus (Lephart et al. 1989). the Caviidae family, even though they are the main source
Lephart et al. (1987), Addo et al. (2007) and Mahoney of food for many predators in South America, and develo-
et al. (2011) described that the first rupture of the vaginal ping for this reason important ecological function (Zogno
closure membrane is positively correlated with the onset et al. 2004).
of puberty in the studied species. Subsequently, the vagi-
nal closure membrane breaks and develops at each estrous CONCLUSIONS
cycle as found in G. spixii, although the corresponding es- By methodology applied in our study, we conclude that
trous phase is not showed in present study. The hormone the estrous cycle of Galea spixii lasts an average of 15.8±1.4
responsible to rupture of vaginal closure membrane is es- days. These results may be helpful for breeding in captivity
tradiol as demonstrated by Deanesly (1966) in ovariecto- and conservation of the species.
mized Cavia porcellus. We also noted the formation and rupture of the vaginal
We believe that future studies could demonstrate the closure membrane, and further studies may reveal the im-
importance of this phenomenon, which was described in portance of this fact for the reproductive success of these
detail in early twentieth century by Stockard & Papanico- rodents.
laou (1917) and Kelly & Papanicolaou (1927) in Cavia por-
Acknowledgements.- To Federal Rural University of Semi-Arid for su-
cellus, but has been little detailed in other rodent species. pplying the animals used in this study; to IBAMA (Brazilian Institute of
To date, we believe that the development of the vaginal Environment and Renewable Resources) for license for captive breeding
closure membrane in G. spixii is possible due to the presen- of the same; and to FAPESP (Fundação de Amparo a Pesquisa do Estado de
ce of the external urethral ostium at the top of the clitoris São Paulo) for financial support.
(Santos et al. 2014b) instead vaginal vestibule, which is ab-
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